Brix et al BMC Plant Biology 2010, 10:23 http://www.biomedcentral.com/1471-2229/10/23 RESEARCH ARTICLE Open Access Can differences in phosphorus uptake kinetics explain the distribution of cattail and sawgrass in the Florida Everglades? Hans Brix1*, Bent Lorenzen1, Irving A Mendelssohn2, Karen L McKee3, ShiLi Miao4 Abstract Background: Cattail (Typha domingensis) has been spreading in phosphorus (P) enriched areas of the oligotrophic Florida Everglades at the expense of sawgrass (Cladium mariscus spp jamaicense) Abundant evidence in the literature explains how the opportunistic features of Typha might lead to a complete dominance in P-enriched areas Less clear is how Typha can grow and acquire P at extremely low P levels, which prevail in the unimpacted areas of the Everglades Results: Apparent P uptake kinetics were measured for intact plants of Cladium and Typha acclimated to low and high P at two levels of oxygen in hydroponic culture The saturated rate of P uptake was higher in Typha than in Cladium and higher in low-P acclimated plants than in high-P acclimated plants The affinity for P uptake was twofold higher in Typha than in Cladium, and two- to three-fold higher for low-P acclimated plants compared to highP acclimated plants As Cladium had a greater proportion of its biomass allocated to roots, the overall uptake capacity of the two species at high P did not differ At low P availability, Typha increased biomass allocation to roots more than Cladium Both species also adjusted their P uptake kinetics, but Typha more so than Cladium The adjustment of the P uptake system and increased biomass allocation to roots resulted in a five-fold higher uptake per plant for Cladium and a ten-fold higher uptake for Typha Conclusions: Both Cladium and Typha adjust P uptake kinetics in relation to plant demand when P availability is high When P concentrations are low, however, Typha adjusts P uptake kinetics and also increases allocation to roots more so than Cladium, thereby improving both efficiency and capacity of P uptake Cladium has less need to adjust P uptake kinetics because it is already efficient at acquiring P from peat soils (e.g., through secretion of phosphatases, symbiosis with arbuscular mycorrhizal fungi, nutrient conservation growth traits) Thus, although Cladium and Typha have qualitatively similar strategies to improve P-uptake efficiency and capacity under low Pconditions, Typha shows a quantitatively greater response, possibly due to a lesser expression of these mechanisms than Cladium This difference between the two species helps to explain why an opportunistic species such as Typha is able to grow side by side with Cladium in the P-deficient Everglades Background The wetland species, Cladium mariscus ssp jamaicense (L.) Pohl (Crantz) K Kenth (sawgrass; hereafter Cladium) and Typha domingensis Pers (cattail; hereafter Typha) are both native to the Florida Everglades and occupy similar habitats [1] Cladium was the dominant plant species in the historical freshwater Everglades, whereas Typha was a minor species occurring in small * Correspondence: hans.brix@biology.au.dk Department of Biological Sciences, Aarhus University, Ole Worms Allé 1, DK8000 Århus C, Denmark and scattered patches throughout the Everglades [2] However, during the past decades Typha has expanded rapidly and replaced thousands of hectares of Cladium marshes and aquatic slough areas in the northern part of the Everglades [3-6] Numerous studies have been conducted to assess the causes and the consequences of this change in vegetation and community structure [7-20], and the driving force for the change appears to be nutrient enrichment, particularly phosphorus (P), from agricultural runoff and Lake Okeechobee outflow [21] © 2010 Brix et al; licensee BioMed Central Ltd This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited Brix et al BMC Plant Biology 2010, 10:23 http://www.biomedcentral.com/1471-2229/10/23 Cladium and Typha are both large, clonal species that can form monospecific communities in freshwater habitats The two species differ, however, in morphology, growth, and life history characteristics [10,15,22] Cladium exhibits many characteristics of adaptation to infertile environments, such as slow growth rate, long leaf longevity, low capacity for nutrient uptake, low leaf nutrient concentrations and a relatively inflexible partitioning of biomass in response to increased nutrient availability [23,24] Typha, on the other hand, has traits of an opportunistic species from nutrient-rich habitats with high growth rates, short leaf longevity, high capacity for nutrient uptake, high leaf nutrient concentrations and flexible biomass partitioning [8,25] Both species are adapted to grow in waterlogged soils by virtue of a well-developed aerenchyma system, but convective gas flow has been documented only in Typha and not in Cladium [26-29] Furthermore, Cladium has lower root porosity and generally higher alcoholic fermentation rates, indicating lower capacity for root aeration than Typha [30] These inherently different traits are considered the main explanation for the rapid spread and competitive success of Typha in the P-enriched areas of the Florida Everglades Cladium and Typha also co-exist in the oligotrophic areas of the Florida Everglades where P availability is extremely low In the interior of Water Conservation Area 2A, an impounded area in the northern Everglades, Cladium and Typha grow together despite soluble P concentrations of less than μg l-1 in the porewaters throughout the soil profile [31] Typha is much less abundant than Cladium and has slow growth rates in these areas [32], and although nutrient enrichment and disturbance around alligator holes have been suggested to favour the proliferation of Typha locally [33], the traits that allow the growth of a high resource-adapted plant like Typha in this low P environment are not understood Studies at high P availability have demonstrated that Typha has a greater relative growth rate, a greater allocation of biomass to leaves, and a lower P-use efficiency than Cladium [10,15,16] In fertile habitats, a high nutrient uptake capacity per unit of root biomass and a high growth rate and biomass allocation to leaves increase the capability to compete for light and reduce the need for a high root biomass However, these traits are not advantageous for growth in a nutrient deficient environment where plants must acquire nutrients at low availability and minimize nutrient losses [34] In such conditions, optimal features would include an extensive root system for soil exploration, a high root surface area (long, thin roots and/or root hairs) for acquisition of nutrients, and efficient mechanisms to capture nutrient ions at low external concentrations [35-37] The main research question we address here is: Which characteristics of Cladium and Typha allow the species Page of 14 to grow in the oligotrophic P-deficient interior of the Florida Everglades, and at the same time explain why Typha out-competes Cladium under P-enriched conditions? As to the second part of the question, abundant evidence in the literature explains how the opportunistic features of Typha can lead to complete dominance in Penriched areas [e.g [7,8,13,15]] Less clear is how Typha can grow and acquire P at the extreme low P-levels prevailing in the unimpacted areas of the Everglades We hypothesized that Typha has a more plastic P uptake system than Cladium in relation to P availability, and this strategy will allow adequate uptake of P and better competitive ability over a wide range of external P concentrations Furthermore, we hypothesized that oxygen-deficient conditions will affect the uptake kinetics of Cladium more than that of Typha, as the latter species has a more efficient system for root aeration (via aerenchyma and internal convective gas flow) These hypotheses were tested in a series of P uptake experiments designed to distinguish differences in P uptake kinetics between the two species Apparent P uptake kinetics were measured for whole plants of Cladium and Typha grown from seeds and acclimated to identical, steady state conditions, in a factorial treatment arrangement with two levels of P (5 and 500 μg P l-1) and two levels of oxygen (8.0 and 0.05) The tissue N concentrations in Cladium were similar (average 10.4 mg g-1 dry weight) in all treatments, and lower overall than in Typha (approximately 17 mg g-1 dry weight), except in the aerated, low-P treatment where plants were smaller (figure 1) The tissue P Brix et al BMC Plant Biology 2010, 10:23 http://www.biomedcentral.com/1471-2229/10/23 Page of 14 Table Plant size Species Oxygen P Leaf length (m) Root length (m) Plant weight (g DW) Root fraction (%) Cladium High oxygen Low 1.01 ± 0.05 0.30 ± 0.03 5.6 ± 0.7 17.4 ± 1.9 High 0.98 ± 0.09 0.50 ± 0.10 7.0 ± 1.9 16.1 ± 1.6 Low oxygen Low High 1.00 ± 0.12 0.95 ± 0.08 0.32 ± 0.04 0.30 ± 0.06 7.0 ± 1.9 12.8 ± 2.9 18.3 ± 2.2 14.1 ± 2.2 High oxygen Low High 0.69 ± 0.12 0.96 ± 0.05 0.48 ± 0.05 0.42 ± 0.06 5.8 ± 0.5 11.6 ± 1.4 22.3 ± 1.9 8.7 ± 1.6 Low oxygen Low 0.96 ± 0.06 0.39 ± 0.03 9.1 ± 1.3 15.1 ± 2.0 High 1.08 ± 0.09 0.29 ± 0.04 23.6 ± 4.3 7.7 ± 0.6 Typha Average (± SE, n = 4-8) leaf and root length, total plant weight and percentage of biomass allocated to roots of the Cladium mariscus spp jamaicense and Typha domingensis plants acclimated to a low and a high P level (5 and 500 μg P l-1) and to aerated and low oxygen conditions (8.0 and